Antibacterial Prenylated Isoflavonoids from the ... - ACS Publications

Article Cite This: J. Nat. Prod. 2018, 81, 1835−1840

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Antibacterial Prenylated Isoflavonoids from the Stems of Millettia extensa Achara Raksat,†,‡ Wisanu Maneerat,†,‡ Raymond J. Andersen,§ Stephen G. Pyne,∥ and Surat Laphookhieo*,†,‡ †

Center of Chemical Innovation for Sustainability (CIS), Mae Fah Luang University, Chiang Rai 57100, Thailand School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand § Department of Chemistry and Department of Earth, Ocean & Atmospheric Sciences, University of British Columbia, 2036 Main Mall, Vancouver, BC, Canada V6T 1Z1 ∥ School of Chemistry, University of Wollongong, Wollongong, New South Wales 2522, Australia

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‡

S Supporting Information *

ABSTRACT: The first phytochemical investigation of the stem extract of Millettia extensa resulted in the isolation and identification of six new isoflavones, millexatins A−F (1−6), together with 16 known compounds. The structures of these new compounds were determined on the basis of their spectroscopic data. Millexatin A (1) is a rare isoflavone containing three isoprenyl units on a modified A ring. Compounds 1, 6, 10, 11, and 14 displayed promising antibacterial activity with MIC values of 2−8 μg/mL.

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he genus Millettia belongs to the family Leguminoseae, which is well known to produce flavonoids, chalcones, rotenoids, and isoflavonoids.1−4 These types of compounds have been recognized to have cytotoxic,3−6 antimalarial,7−9 and anti-inflamatory5,10,11 activities. Some species of Millettia have been utilized as traditional medicines to treat various diseases including dysmenorrhea, rheumatic pain, paralysis, snakebites, insect bites, and inflammation.12−14 Millettia extensa (Benth.) Baker is a large climbing shrub that is distributed mainly in the northern part of Thailand. According to the information from the SciFinder Scholar database (Chemical Abstracts Service, Columbus, OH, USA), no phytochemical investigation or biological evaluation of this plant has been reported, and its crude acetone extract showed good antibacterial activities. This information led us to investigate antibacterial compounds from this plant. Six new isoflavonoids (1−6) together with 16 known compounds and antibacterial activities of some isolated compounds are described in this paper. © 2018 American Chemical Society and American Society of Pharmacognosy

RESULTS AND DISCUSSION

The extract of the stems of M. extensa was subjected to purification by repeated column chromatography (CC), which led to the isolation and elucidation of 19 isoflavones (1−19), two rotenoids (20 and 21), and a pterocarpan (22). By comparing their physical and spectroscopic data with published values, known compounds (7−22) were identified as 3′-methylorobol (7),15 7,4′-di-O-prenylgenistein (8),16,17 5hydroxy-7-methoxy-4′-O-(3-methylbut-2-enyl)isoflavone (9),18 auriculatin (10),19,20 scandenone (11),21,22 5-O-methyl4′-O-(3-methyl-2-butenyl)alpinumisoflavone (12),23 elongatin (13),24 auriculasin (14),20,21 2′-O-methylisoauriculatin (15),22 4′-methylalpinumisofiauone (16),25 2′-deoxyisoauriculatin (17),22 isoauriculasin (18),20 isoauriculatin (19),20,26 (−)-sumatrol (20),19 (−)-6a,12a-dehydrotoxicarol (21),27 and (−)-maackiain (22).28 Millexatin A (1) exhibited an ion peak at m/z 491.2447 ([M + H]+, calcd 491.2434) in its HRESITOFMS data, which Received: April 23, 2018 Published: August 14, 2018 1835

DOI: 10.1021/acs.jnatprod.8b00321 J. Nat. Prod. 2018, 81, 1835−1840

Journal of Natural Products

Article

Chart 1

Table 1. 1H NMR (600 MHz) Spectroscopic Data of Millexatins A−F (1−6) in CDCl3 (δ in ppm, J in Hz) 1a

position 2 8 3′ 5′ 6′ 1″ 2″ 4″ 5″ 1‴ 2‴ 3‴ 4‴ 5‴ 1⁗ 2⁗ 4⁗ 5⁗ OH-5 OMe-5 OH-2′ OMe-2′ OH-4′ OMe-5′

8.12, s 6.59, 6.55, 7.01, 3.11, 5.08, 1.75, 1.67, 2.90, 2.65, 4.68,

d (2.0) dd (8.5, 2.0) d (8.5) d (7.0) t (7.0) s s dd (13.7, 7.0); dd (13.7, 7.0) t (7.0)

1.55, s 1.51, s 2.90, dd (13.7, 7.0); 2.65, dd (13.7, 7.0) 4.68, t (7.0) 1.55, s 1.51, s 12.43, s 5.50, br s

2 7.89, 6.70, 6.68, 6.65, 7.03, 6.78, 5.79, 1.51, 1.51, 4.54,

s s d (2.5) dd (8.6, 2.5) d (8.6) d (10) d (10) s s d (7.0)

3

4

7.80, s 6.63, s 6.64, s

7.87, s 6.67, s 6.58, s

6.92, 6.76, 5.74, 1.50, 1.50, 4.65,

6.93, 6.74, 5.76, 1.49, 1.49,

s d (10.0) d (10.0) s s

6.18, 5.29, 5.35, 1.43, 1.43,

dd (17.6, 10.4) d (10.4); d (17.6) s s

s d (10.0) d (10.0) s s d (6.6)

5.53, t (7.0)

5.55, t (6.6)

1.82, s 1.77, s

1.81, s 1.79, s

3.93, s 9.34, s

3.91, s

6a

5 7.81, s

7.96, s

6.54, 6.42, 6.94, 6.62, 5.65, 1.53, 1.53, 6.72,

6.56, 6.48, 7.00, 3.37, 5.22, 1.84, 1.71, 6.71,

d (2.5) dd (8.3, 2.5) d (8.3) d (10.0) d (10.0) s s d (10.0)

d (2.5) dd (8.4, 2.5) d (8.4) d (7.3) br t (7.3) s s d (10.0)

5.65, d (10.0)

5.62, d (10.0)

1.50, s 1.50, s

1.49, s 1.49, s

12.56, s 3.90, s 8.99, s

9.44, br s

8.50, s

5.90, s

5.00, br s

5.09, s

3.75, s 7.94, s 3.85, s

a

Recorded at 400 MHz.

compound 1 is an isoflavanone. Compound 1 showed 1H NMR resonances for a H-bonded hydroxy proton, an olefinic proton, characteristic of isoflavanones, spin-coupled ABC-type aromatic protons, an isoprenyl unit, and a germinal diisoprenyl group (Table 1). The germinal diisoprenyl unit was placed at

indicated a molecular formula of C30H34O6. Analysis of the NMR spectroscopic data of 1 indicated it is related in structure to isoxantholupon,29 with a modified A ring. The major difference between of these two compounds found was that the core structure of isoxantholupon is a flavanone, while that in 1836



Article

Figure 1. Selected HMBC correlations (1H → 13C) of compounds 1−6.

Table 2. 13C NMR (150 MHz) Spectroscopic Data of Millexatins A−F (1−6) in CDCl3 (δ in ppm)

C-8 due to the HMBC correlations (Figure 1) of H-1‴/H-1⁗ (δH 2.90 and 2.65) with C-7 (δC 194.6), C-8 (δC 57.0), and C9 (δC 174.6), whereas the isoprenyl group was placed at C-6 from of the HMBC correlation of H-1″ (δH 3.11) with C-5 (δC 162.7), C-6 (δC 116.1), and C-7 (δC 194.6). It should be noted that griffonianone C30 is the first example of an isoflavone with a modified A ring and was isolated from M. grif foniana by Yankep et al. in 2001. However, millexatin A is a rare isoflavone containing three isoprenyl units on a modified A ring. Millexatin B (2), molecular formula C26H26O6, was determined from its HRESITOFMS data ([M + H]+ m/z 435.1804, calcd 435.1808). The NMR spectroscopic data (Table 1) displayed characteristic resonances for a tetraoxygenated isoflavone similar to those of isoauriculatin22 isolated from the leaf extract of Millettia auriculata. The major distinction was the replacement of a H-bonded hydroxy group at C-5 in isoauriculatin22 with a methoxy group in 2. The HMBC correlation between the methoxy protons (δH 3.93) and the olefinic proton H-1″ (δH 6.78) with C-5 (δC 155.0) further verified this deduction. Millexatin C (3) was deduced to have a molecular formula of C28H30O7 from its HRESITOFMS data ([M + H]+ m/z 479.2055, calcd 479.2070). Analysis of the NMR spectroscopic data of 3 (Tables 1 and 2) revealed that it is structurally related to millexatin B (2). The major difference between these two compounds was found on ring B. Compound 2 showed ABCtype, spin-coupled aromatic protons, while compound 3 exhibited signals for two singlet para-aromatic protons at δH 6.64 and 6.92 and for an additional methoxy group at δH 3.75. These resonances were assigned to H-3′, H-6′, and OMe-2′, respectively, which were further supported from the following NOESY cross-peaks (Figure 1): OMe-5′ (δH 3.85) with H-6′ (δH 6.92) and OMe-2′ (δH 3.75) with H-3′ (δH 6.64). Millexatin D (4) had a molecular formula of C26H26O6, which was deduced from its HRESITOFMS data ([M + H]+ m/z 435.1804, calcd 435.1808). The NMR spectroscopic data of 4 were similar to those of 2, except for the absence of resonances for an isoprenyloxy unit and H-5′ in 4 (Tables 1 and 2). The 1H NMR spectrum of 4 showed resonances for a 1,1-dimethylallyl group. This unit was attached at C-5′, most likely formed via the Claisen rearrangement of the isoprenyl

a

position

1a

2

3

4

5

6a

2 3 4 5 6 7 8 9 10 1′ 2′ 3′ 4′ 5′ 6′ 1″ 2″ 3″ 4″ 5″ 1‴ 2‴ 3‴ 4‴ 5‴ 1⁗ 2⁗ 3⁗ 4⁗ 5⁗ OMe-5 OMe-2′ OMe-5′

154.1 129.0 179.6 162.7 116.1 194.6 57.0 174.6 114.4 110.8 159.1 106.7 157.6 109.1 130.9 21.0 121.5 131.9 17.9 25.8 38.8 116.7 136.0 25.7 17.8 38.8 116.7 136.0 25.7 17.8

152.0 125.0 178.0 155.0 113.6 158.6 99.9 157.9 111.4 113.5 157.3 104.3 160.5 107.8 130.3 115.0 130.0 77.6 27.9 27.9 64.4 119.0 138.0 25.4 17.7

151.9 122.0 174.4 155.2 112.8 157.4 99.5 158.2 112.7 111.8 151.2 100.2 148.4 143.0 115.1 115.7 130.2 77.2 27.8 27.8 65.6 119.6 137.2 25.4 17.8

152.4 125.3 177.8 155.1 113.5 158.5 99.9 158.0 111.6 113.1 156.1 107.7 156.4 124.6 127.2 115.3 130.7 76.9 27.9 27.9 39.2 147.4 113.1 26.7 26.7

151.8 124.9 178.4 154.1 107.5 152.7 101.4 152.0 107.7 113.2 157.5 105.6 157.3 107.4 130.3 115.1 128.2 77.7 27.8 27.8 114.5 127.2 78.0 27.3 27.3

154.4 123.0 182.0 158.8 113.6 158.1 100.6 150.3 104.9 112.6 157.1 106.3 158.2 108.6 130.5 21.3 121.6 131.9 17.7 25.7 114.6 127.2 78.3 28.0 28.0

62.5

62.3 56.2 56.1

62.6

Recorded on 100 MHz.

unit of compound 2. The HMBC correlations also supported this assignment. 1837



Article

Scheme 1. Plausible Biosynthetic Pathways for Compounds 1−6

Table 3. Antibacterial Activity of Compounds 1, 6, 7, 10, 11, 13, 14, 17, 19, 20, and 22 MIC (μg/mL) Gram-positive bacteria

Gram-negative bacteria

compound

S. aureus TISTR 1466

S. epidermidis ATCC 12228

B. subtilis TISTR 008

S.typhimurium TISTR781

Ps. aeruginosa TISTR 292

1 6 7 10 11 13 14 17 19 20 22 vancomycin gentamycin

2 2 32 2 2 inactive 4 inactive inactive inactive inactive 0.25 not tested



128 128 128 128 128 128 128 128 128 128 128 not tested 0.25

128 128 128 128 128 128 128 128 128 128 128 not tested 2

Inactive at >128 μg/mL.

a

Millexatin E (5) had a molecular formula of C25H22O6, which was deduced from its HRESITOFMS data ([M + H]+ m/z 441.1332, calcd 441.1314). The NMR spectroscopic data (Tables 1 and 2) were similar to those of auriculatin (10), having a 1,2,4-trisubstituted B ring. However, compound 5 showed resonances for two pyran rings that were located at C5/C-6. Correlations in the HMBC spectrum between H-1″ (δH 6.62) and C-5 (δC 154.1), C-6 (δC 107.5), and C-7 (δC 152.7) and between H-1‴ (δH 6.72) and C-7 (δC 152.7), C-8 (δC 101.4), and C-9 (δC 152.0) supported the location of these two pyran rings. Millexatin F (6) had a molecular formula of C25H24O6, which was determined from its HRESITOFMS data ([M + H]+ m/z 421.1660, calcd 421.1651). The NMR spectroscopic data (Tables 1 and 2) were very similar to those of millexatin E (5), except for the absence of resonances for a pyran ring at C5/C-6. Compound 6 showed additional resonances for an isoprenyl unit and a H-bonded hydroxy group (δH 12.56) at C5. The HMBC spectrum showed correlations of OH-5 (δH 12.56) with C-5 (δC 158.8), C-6 (δC 113.6), and C-10 (δC 104.9) and of H-1″ (δH 3.37) with C-5 (δC 158.8), C-6 (δC

113.6), and C-7 (δC 158.1). Thus, the structure of 6 was elucidated as shown. This structure was found in the SciFinder Scholar database (Chemical Abstracts Service, Columbus, OH, USA), but no references were indicated for this compound, suggesting that it is new. Putative biogenetic pathways toward the generation of the isoflavones 1−6 are shown in Scheme 1. The intermediate 23.1 could be generated from isoflavone 23 (not isolated from this study) via prenylation at C-8. Futher prenylation at C-8 of intermediate 23.1 would give compound 1. Compound 6 could be also obtained from intermediate 23.1 via cyclization of the isoprenyl group at C-8 onto the OH-7 group. A second cyclization between the isoprenyl group at C-6 and a OH-5 group of compound 6 would give compound 5. A regioselective methylation of the OH-5 followed by cyclization of the isoprenyl group at C-6 with the OH-7 group would give intermediate 23.2. This upon selective O-prenylation at C-4′ would produce compound 2. Claisen rearrangement of 2 could generate compound 4.31 Finally, oxidation of compound 2 at C-5′ followed by O-dimethylation would then give compound 3. 1838



Article

Antibacterial Assay. All bacterial strains used in these experiments were obtained from the Microbiological Resources Center, Bangkok, Thailand. The antibacterial assay was determined as recommended by Clinical and Laboratory Standards Institute.34−36

Most of the isolated compounds obtained were evaluated for their antibacterial activity against three Gram-positive and two Gram-negative bacteria, as summarized in Table 3. Compounds 1, 6, 10, 11, and 14 showed potent antibacterial activity against Gram-positive bacteria with MIC values ranging from 2 to 8 μg/mL. Compound 7 showed moderate activity against S. aureus with a MIC value of 32 μg/mL. All remaining compounds showed either weak (MIC 64−128 μg/ mL) or no perceptible antibacterial activity against all tested bacterial strains.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jnatprod.8b00321. HRESITOFMS and 1D and 2D NMR spectra of new compounds 1−6 (PDF)

EXPERIMENTAL SECTION

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General Experimental Procedures. The general information on instruments and materials was the same as in previous reports.32−35 Plant Material. The stems of M. extensa were obtained in January 2017 from Donmoon Village, Silaphet Subdistrict, Pua District, Nan Province, Thailand. Plant authentication was verified by Mr. Martin Van de Bult, and a voucher specimen (MFU-NPR0165) was deposited at the Natural Products Research Laboratory of Mae Fah Luang University. Extraction and Isolation. The chopped and dried stems of M. extensa (1.2 kg) were extracted with acetone (6 L) at room temperature (3 days × 2) and concentrated under reduced pressure to give an acetone extract (194.0 g). The crude extract (76.8 g) was subjected to CC over silica gel, eluting with 100% hexanes to 100% acetone, to give six fractions (F1−F6). Fractionation of F3 (1.08 g) by Sephadex LH-20 (8:2 MeOH−CH2Cl2) gave three subfractions (F3A−F3C). Purification of F3C (124.3 mg) by CC (1:9 EtOAc− hexanes) yielded compounds 8 (1.4 mg), 9 (1.5 mg), 16 (1.7 mg), 17 (22.0 mg), 18 (1.8 mg), and 19 (4.5 mg). Purification of F4 (639.8 mg) by CC (1.5:8.5 EtOAc−hexanes) gave compounds 4 (3.7 mg), 5 (1.8 mg), and 15 (2.7 mg). Fractionation of F5 (13.4 g) by Sephadex LH-20 (9:1 MeOH−CH2Cl2) gave four subfractions (F5A−F5D). Separation of F5A (2.7 g) by CC (2:8 acetone−hexanes) yielded compounds 1 (18.0 mg), 2 (2.3 mg), 3 (3.1 mg), and 12 (7.2 mg). Purification of F5C (8.4 g) by CC (2:8 EtOAc−hexanes) yielded compounds 10 (2.2 g), 11 (1.3 g), 13 (25.9 mg), 14 (2.3 mg), 20 (15.2 mg), and 21 (2.5 mg). Compounds 6 (471.0 mg), 7 (7.3 mg), and 22 (41.3 mg) were obtained from F5D (950.1 mg) by CC (0.2:9.8 MeOH−CH2Cl2). Millexatin A (1): yellow, viscous oil; UV (MeOH) λmax (log ε) 203 (4.28), 269 (3.93), 349 (3.22) nm; IR (neat) νmax 3373, 2967, 1669, 1621, 1547, 1447 cm−1; 1H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/z 491.2447 [M + H]+ (calcd for C30H35O6, 491.2434). Millexatin B (2): yellow viscous oil; UV (MeOH) λmax (log ε) 203 (4.15), 225 (3.98), 268 (4.07), 331 (3.38) nm; IR (neat) νmax 3382, 2924, 1607, 1582, 1467 cm−1; 1H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/z 435.1804 [M + H]+ (calcd for C26H27O6, 435.1808). Millexatin C (3): yellow solid, mp 112−115 °C; UV (MeOH) λmax (log ε) 272 (4.33), 335 (3.49) nm; IR (neat) νmax 2976, 1639, 1511, 1466 cm−1; 1H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/ z 479.2055 [M + H]+ (calcd for C28H31O7, 429.2070). Millexatin D (4): yellow, viscous oil; UV (MeOH) λmax (log ε) 291 (4.23), 334 (3.63) nm; IR (neat) νmax 3335, 2973, 1608, 1467 cm−1; 1 H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/z 435.1804 [M + H]+ (calcd for C26H27O6, 435.1808). Millexatin E (5): yellow, viscous oil; UV (MeOH) λmax (log ε) 296 (4.20), 333 (3.46) nm; IR (neat) νmax 3338, 2976, 1615, 1570, 1366 cm−1; 1H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/z 441.1332 [M + Na]+ (calcd for C25H22NaO6, 441.1314). Millexatin F (6): yellow solid, mp 218−219 °C; UV (MeOH) λmax (log ε) 202 (4.07) 272 (4.17), 359 (2.91) nm; IR (neat) νmax 3349, 2976, 1639, 1429 cm−1; 1H and 13C NMR, see Tables 1 and 2; HRESITOFMS m/z 421.1660 [M + H]+ (calcd for C25H25O6, 421.1651).

AUTHOR INFORMATION

Corresponding Author

*Tel: +66-5391-6238. Fax: +66-5391-6776. E-mail: surat.lap@ mfu.ac.th (S. Laphookhieo). ORCID

Raymond J. Andersen: 0000-0002-7607-8213 Stephen G. Pyne: 0000-0003-0462-0277 Surat Laphookhieo: 0000-0002-4757-2781 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We are grateful to the Thailand Research Fund and Mae Fah Luang University for financial support (BRG5980012). We thank Mr. M. Van de Bult for the plant identification and Ms. P. Meesakul and Mr. W. Jaidee for recording the NMR spectra.

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